Most Genomic Loci Misrepresent the Phylogeny of an Avian Radiation Because of Ancient Gene Flow

Phylogenetic trees based on genome-wide sequence data may not always represent the true evolutionary history for a variety of reasons. One process that can lead to incorrect reconstruction of species phylogenies is gene flow, especially if interspecific gene flow has affected large parts of the genome. We investigated phylogenetic relationships within a clade comprising eight species of passerine birds (Phylloscopidae, Phylloscopus, leafwarblers) using one de novo genome assembly and 78 resequenced genomes. Onthe basis of hypothesis-exclusion trials based on D-statistics, phylogenetic network analysis, and demographic inference analysis, we identified ancient gene flow affecting large parts of the genome between one species and the ancestral lineage of a sister species pair. This ancient gene flow consistently caused erroneous reconstruction of the phylogeny when using large amounts of genome-wide sequence data. In contrast, the true relationships were captured when smaller parts of the genome were analyzed, showing that the "winner-takes-all democratic majority tree" is not necessarily the true species tree. Under this condition, smaller amounts of data may sometimes avoid the effects of gene flow due to stochastic sampling, as hidden reticulation histories are more likely to emerge from the use of larger data sets, especially whole-genome data sets. In addition, we also found that genomic regions affected by ancient gene flow generally exhibited higher genomic differentiation but a lower recombination rate and nucleotide diversity. Our study highlights the importance of considering reticulation in phylogenetic reconstructions in the genomic era